SLEEP PATTERNS are developmental (Owens & Palermo, 2008). Infancy is a time of rapid consolidation of nighttime sleep (Henderson, France, Owens, & Blampied, 2010; Owens & Palermo, 2008; Sadeh, Mindell, Luedtke, & Wiegand, 2009), whereas adolescence is characterized by circadian rhythm cycle changes (Carskadon, Acebo, & Jenni, 2004). Sleep problems are also developmental. Among infants and toddlers, behavioral insomnias of childhood (BIC) and sleep disordered breathing (SDB) disorders, (ie, a continua from snoring to obstructive sleep apnea) are the most common (Jan et al., 2010). Both BIC and SDB cause disrupted and/or inefficient sleep.
Left untreated, chronic sleep disorders may lead to impaired brain development, neuronal damage, and permanent loss of developmental potentials (Jan et al., 2010). Nearly all neurobehavioral and neurocognitive conditions of childhood are potentially linked to sleep problems; this link is likely to be bidirectional (Dorris, Scott, Zuberi, Gibson, & Espie, 2008). For example, SDB is associated with impaired executive function in preschoolers (Aronen et al., 2009), while nonrespiratory sleep problems were significantly associated with lack of cognitive and emotional readiness for first grade (Ravid, Afek, Suraiya, Shahar, & Pillar, 2009). For children in the Individuals with Disabilities and Education Act (IDEA) Part C/Early Intervention (EI) and Part B/Early Childhood Special Education (ECSE) programs, (Individuals with Disabilities Education Improvement Act of 2004) there are potential risks to at least three of the developmental domains used to establish eligibility for those programs: behavior, cognition, and physical development (Montgomery & Dunne, 2007; Touchette, Petit, Tremblay, & Montplaisir, 2009).
Behavioral insomnias of childhood affect 40% to 75% of children with developmental delays, which is two to three times the rate among typically developing children (Couturier et al., 2005; Krakowiak, Goodlin-Jones, Hertz-Picciotto, Croen, & Hansen, 2008). This etiology may involve intrinsic abnormalities in sleep regulation and circadian rhythms, cognitive delays, sensory deficits, medications used to treat associated symptoms, or increased parental stress. Sleep disordered breathing, unlike BIC, is a manifestation of anatomical processes, local tissue compliance, and neurophysiology (Beebe, 2006; Schechter, 2002). Sleep disordered breathing symptoms peak in the first 6 years of life, at approximately 2% for apnea and approximately 20% for snoring in the general population (Bonuck et al., 2011), given the relative adenotonsillar hypertrophy at these ages (Halbower & Marcus, 2003). Sleep disordered breathing–related morbidity includes delayed developmental milestones (Calhoun et al., 2010), speech-language impairments (de Serres et al., 2002; Lundeborg, McAllister, Samuelsson, Ericsson, & Hultcrantz, 2009), behavioral (Beebe, 2006) and cognitive (Bass et al., 2004) effects, and growth failure (Bonuck, Parikh, & Bassila, 2006). The prevalence of SDB is high in certain congenital (eg, Down syndrome) (Ng et al., 2006) and neuromuscular (Arens & Muzumdar, 2010) conditions, though prevalence across the spectrum of children with developmental disorders is unknown.
To date, just a few studies have examined sleep problems among children in early intervention or special education programs (vs children selected for specific conditions) (Goodlin-Jones, Tang, Liu, & Anders, 2008) or as part of a larger study on at risk children (Matson, Fodstad, & Mahan, 2009). In one study, both BIC and SDB were more common among 4 to 5 year olds with significant intellectual and/or physical disabilities attending specialized schools versus children in mainstream schools in terms of “settling” down to sleep (62% vs 23%), night waking (46% vs 31%), loud snoring (27% vs 14%), and parental cosleeping (29% vs 10%) (Quine, 2001). In another study, sleep problems were found to be more common among children attending behavior/conduct programs versus matched controls (Blunden & Chervin, 2008). Finally, a community sample of 24 month olds found that those with language delays had significantly more “sleep problems” than those without language delays (Carson, Klee, Perry, Muskina, & Donaghy, 1998).
Given the symptom overlap between sleep problems and developmental disorders, early detection is critical. Ideally, this would occur as part of developmental surveillance in primary care (Duby et al., 2006). Yet, sleep problems are underdiagnosed in routine pediatric care compared with parental perception (Chervin, Archbold, Panahi, & Pituch, 2001), and epidemiologic prevalence data (Meltzer, Johnson, Crosette, Ramos, & Mindell, 2010). This is unfortunate, given that a range of interventions, if timely, are often effective. Cognitive/behavioral interventions for BIC include a range of extinction programs (Galland & Mitchell, 2010; Morgenthaler et al., 2006). Most are efficacious. In a recent review, 94% were efficacious, with 80% of children retaining improvements 3 to 6 months later. Compared to drug treatments, behavioral interventions are more effective in the short- and long-term (Ramchandani, Wiggs, Webb, & Stores, 2000) and address behavioral aspects of the problem (Wiggs, 2009). Likewise, for SDB, multiple reviews find significant improvements in behavior, cognition (Garetz, 2008; Mitchell & Kelly, 2006), and growth (Bonuck, Freeman, & Henderson, 2009) following adenotonsillectomy.
In children with developmental delays and disabilities, providers (and parents) often view sleep problems not as a distinct disorder, but rather as part of the primary developmental disorder. As a result, sleep problems in these children are rarely assessed as a distinct domain (Dorris et al., 2008), resulting in significant unmet treatment need (Wiggs & Stores, 1996). Although effective behavioral interventions exist (see earlier), the American Academy of Sleep Medicine (2006) cites the need for additional studies to “...examine the use of these strategies in children with special needs (e.g., children with autism spectrum disorders, mental retardation, neuro-developmental disabilities) and in children with chronic medical and psychiatric conditions” (Morgenthaler et al., 2006, p. 1280). While research is emerging on effective treatment of sleep problems among children on the autism spectrum, there is little research on the effectiveness of behavioral interventions in children with other developmental delays/disabilities. To our knowledge, there are just two such small studies, in England (Montgomery, Stores, & Wiggs, 2004; Wiggs & Stores, 1998). In these trials of children with concurrent severe BIC and severe learning disabilities, behavioral intervention resulted in significant and sustained improvements, with the authors concluding that “the behavioral approach to treatment used for children without learning disabilities is acceptable for use in this population” (Wiggs & Stores, 1998).
Sleep-related data, when it is collected, is generally used for background rather than screening or prognostic purposes. Furthermore, instruments used in EI are validated for outcomes other than sleep disorders. Given the underrecognition of sleep problems in primary care, a parallel lack of recognition in the early intervention field is not surprising. To date, there has not been a systematic review of developmental screening and assessment instruments (hereafter “instruments”) to determine the extent to which they ask about sleep problems, including whether any incorporate validated pediatric sleep questionnaires identified by sleep medicine researchers (Lewandowski, Toliver-Sokol, & Palermo, 2011; Spruyt & Gozal, 2011). Such a review is a necessary first step. General background questions about sleep, which may be asked during an evaluation, are likely to be inadequate for the purposes of determining whether a child has or needs a referral for a clinically significant sleep disorder.
Toward promoting early detection of sleep problems in children with developmental disorders, we undertook a systematic review of developmental instruments' inclusion of items related to both SDB and BIC. The goals of this review were to (a) develop a catalogue of general or multidomain instruments that clinicians and EI and ECSE programs routinely employ, (b) identify if and how these instruments incorporate BIC and/or SDB-related items, (c) classify these items by the dimension of sleep behavior they assess (eg, night waking, sleep resistance), and (d) determine whether any instruments are satisfactory for screening for BIC or SDB, compared with items in validated pediatric sleep questionnaires.
We identified lists and compendia of instruments used to assess general development and social-emotional development in children within the age range of the IDEA EI and ECSE programs, that is, birth through 60 months. To identify these instruments, we conducted a search of the terms “developmental screening” or “developmental assessment” and “instruments” in PubMed, ERIC, Psycinfo, CINAHL, and Google for the years 2000–2010. Data saturation was reached at 38 sources, shown in the Appendix.
Figure 1 shows a flowchart of instrument lists and instruments identified. On the basis of compendia or publisher descriptions, we identified unique instruments from these 38 that (a) assessed either social-emotional or adaptive functioning, or behavior or temperament; (b) employed parent/caregiver direct report; and (c) were used for children in the 0- to 60-month age range. We excluded instruments used solely to screen or assess (a) mental health (ie, depression, conduct disorder); cognition, or speech/language; (b) a specific diagnosis (eg, autism), or (c) home or family functioning or environment. This process yielded 101 instruments, 36 of which appeared in only one source. For streamlining purposes, we eliminated all but 2 of these 36, on the basis of RB's (a developmental psychologist) experience of those 2 instruments as being used in practice, resulting in 67 instruments. Of the 67 instruments, 20 were age-related variations on a core instrument—that is, there are 7 different age versions of the Ages and Stages Questionnaires: Social-Emotional (available from authors). We attempted to directly view all instruments. For those we could not view directly, we asked staff at the National Early Childhood Technical Assistance Center (NECTAC), or the publisher, to read us the items (preferred), or indicate if there were any related to our search terms, which were: “sleep(y)(iness)”, “wake”, “night(time)”, “bed(time)”, “fatigue”, “nap”, “snore/snoring” or “tired(ness).”
The authors developed an abstracting instrument (Figure 2), which they employed to classify SDB- and/or BIC-related items; copyright restrictions preclude us from reprinting items. Snoring or apnea items were classified as SDB. To classify BIC items, we used categories listed in the Children's Sleep Habits Questionnaire (Owens, Spirito, & McGuinn, 2000), which correspond to sleep-disorder diagnoses (American Academy of Sleep Medicine, 2006). Categories included bedtime resistance, sleep onset delay, sleep duration, sleep anxiety, and night waking. In addition, we included non-BIC categories from the Children's Sleep Habits Questionnaire: parasomnias (nightmares, sleep-walking), daytime sleepiness, parental concerns about their child's sleep, nighttime sleep consolidation, and 24-hour sleep duration. The latter were included to cover the full range of pediatric sleep disorders. We assigned the following quality indicators to each instrument: A = Direct, reviewed by authors; B = Indirect, reviewed by librarian or colleague; C = Indirect, reviewed by publisher for search terms; D = Indirect, information gleaned from Web site; or E = No information.
Two teams of the authors—a professor working with an undergraduate research intern and two Master's level researchers working together—independently abstracted information. The two team's initial classifications were in more than 80% agreements. After discussions to reconcile differences, the remaining unresolved classifications (12% of total and 11% of unique instruments) were discussed with a fifth author, a developmental psychologist, until consensus was achieved. The following guidelines were used for abstracting: (a) teacher/childcare provider items were excluded, given our primary focus on nighttime sleep and secondary focus on 24-hour sleep patterns; (b) nap items were included only if there was a statement about frequency, and in this case they were classified under “sleep duration”; (c) items that satisfied criteria for two BIC categories were classified in both, for example, a question about needing a parent in the room to fall asleep was classified as “sleep anxiety” and “bedtime resistance,” and (d) different age versions of the same instrument were abstracted separately.
We conducted a separate analysis of sleep-related items in the most commonly used instruments in EI/ECSE programs. These were identified by other researchers to measure progress toward outcomes related to social-emotional skills, knowledge and skill acquisition and use, and use of appropriate behaviors to meet needs. (Hebbeler, Mallik, & Kahn, 2008).
Data were entered and analyzed in Microsoft Office Excel (version 2007; Redmond, Washington).
Characteristics of the 67 total (ie, counts multiple-age versions separately) and 47 unique instruments included in the review are shown in Table 1. The authors directly examined 71% of total and 60% of unique instruments. The mean number of sleep-related items was 1.5. Overall, 38% (26/67) of total and 47% (22/47) of unique instruments contained no sleep-related items. None included any SDB items, for example, pertaining to snoring or apnea.
The frequency and types of BIC items are shown in Table 2. Among the 47 unique instruments, the 3 most common item types were: (1) resistance to bedtime, (2) night waking (each included on 21% of instruments), and (3) parental concerns about their child's sleep (≥1 item on 19% of instruments). Among the few instruments addressing these issues, most had only one such item. Finally, only 2 instruments (4%) asked parents about daytime sleepiness even though such fatigue might not only be a clear manifestation of nighttime sleep problems but can also contribute to daytime behavioral and cognitive disturbances.
We examined the frequency and type of sleep-related items in the most commonly used instruments in state EI and ECSE programs (Hebbeler et al., 2008) (Table 3). Again, none included any SDB-related items. The Battelle was the most commonly used, and had the most (n = 6) BIC items, followed by the Bayley (n = 3), and the Hawaii Early Learning Profile (n = 2). Overall, 70% (7/10) of these commonly used instruments included 1 or less sleep-related item.
We reviewed 47 unique and 67 total (multiple age versions of unique) instruments used by EI/ECSE programs to determine whether and how they screened for behavioral (BIC) and respiratory-related (SDB) sleep disorders. About half did not ask any BIC-related items; of those that did, there were a mean of 1.5 items. Particularly troubling is the fact that there was not one SDB-related item on any of the instruments. Given the significant “shared co-morbidity” between sleep problems and developmental disorders (Bonuck & Grant, in press), our findings have implications for early intervention programs. In particular, since 2005, EI/ECSE programs must report on progress related to developmental domains that both BIC and sleep problems affect (a) positive social-emotional skills (including social relationships), (b) knowledge and skill acquisition and use (eg, early language/communication/literacy), and (c) use of appropriate behaviors to meet their needs (Early Childhood Outcomes Center, 2011). Thus, without systematic assessment of sleep problems, employing items and/or instruments validated for that purpose, the field of early intervention will underascertain remediable risk factors for delayed development.
The promise of early intervention resides in the efficacy of identifying and treating problems during the sensitive and responsive periods of early development. There is significant evidence that treatment of early childhood sleep problems is efficacious, via modifiable parental behaviors, for example, removing parental presence at sleep onset is associated with less fragmented (Touchette et al., 2005) and longer duration (Touchette et al., 2009) of sleep. Furthermore, American Academy of Sleep Medicine (2006) protocols to prevent these types of problems are effective, and generally not difficult to impart to parents, though further research is required on their effectiveness in children with developmental disorders (Morgenthaler et al., 2006). Furthermore, there is significant overlap between behavioral and respiratory-related sleep issues (Blunden & Beebe, 2006): with an estimated 40% to 50% of children referred for polysomnographic evaluation of suspected SDB presenting with comorbid behavioral sleep disorders (Byars, Apiwattanasawee, Leejakpai, Tangchityongsiva, & Simakajornboom, 2011; Meltzer, Moore, & Mindell, 2008).
Early intervention professionals may wish to consult 2 recent reviews of pediatric sleep questionnaires (Lewandowski et al., 2011; Spruyt & Gozal, 2011). It is beyond the scope of this article to cross-reference the items in those reviews with the items in the instruments we reviewed. For BIC, on the basis of those reviews, questionnaires to consider are the Tayside Children's Sleep Habits Questionnaire (McGreavey, Donnan, Pagliari, & Sullivan, 2005), the Brief Infant Sleep Questionnaire (Sadeh, 2004), or the Children's Sleep Habits Questionnaire (CSHQ)—Preschool version (Goodlin-Jones, Sitnick, Tang, Liu, & Anders, 2008). In Table 2, CSHQ items omit the 8 pertaining to morning waking, and the 7 related to daytime sleepiness given our focus on nighttime sleeping. For SDB, the Pediatric Sleep Questionnaire validated in 2- to 18-year olds against overnight sleep studies (polysomnography), fulfilled each of the 11 psychometric testing requirements except for standardization and norms (Spruyt & Gozal, 2011). Aside from one exception for the CSHQ (Goodlin-Jones, Tang, et al., 2008), none of the questionnaires were purposefully validated in children with developmental disability and delay, though children who would meet EI/ECSE eligibility criteria are likely among those evaluated with these instruments.
Limitations of the current review include our inability to view all instruments (we directly examined 71% of the total instruments) and the fact that the instruments reviewed were designed for purposes other than the assessment of sleep, and as such were not validated for that purpose. We also limited our focus to nighttime sleep behaviors and focused on total sleep, including naps, as a secondary measure. While we made this decision given that the former appears to be more critical in the development of cognitive function (Lam et al., 2011), we may have overlooked important information regarding daytime sleep.
Pediatric sleep problems have documented adverse effects upon behavior, cognition, and growth and thus have implications for the developmental domains targeted by EI and ECSE programs. Yet, about half of current instruments used to assess eligibility in EI/ECSE programs do not systematically address BIC, and none address sleep disordered breathing. Research is needed on the effectiveness of screening and intervention for both behavioral and respiratory sleep problems within the heterogeneous EI and ECSE populations using validated pediatric sleep questionnaires.
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Appendix: List of Data Sources Used to Identify Instruments for Review
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behavioral insomnia; developmental delay; developmental disability; children; early intervention; sleep disordered breathing; sleep disorders